Prevalence of Intestinal Parasitic Infection among Pre-School and School-Aged Children Attending to Fann University Hospital, Dakar: Results from Retrospective Analysis ()
1. Introduction
Morbidity related to intestinal parasitic infection caused by pathogenic protozoa and helminths is important worldwide, particularly in developing countries where children are most affected. It is estimated that 3.5 billion patients are affected and that 450 million of them are ill [1]. According to World Health Organization (WHO), children living in endemic are most affected with an estimated number of 270 million preschool children and over 600 million school children [2]. Among intestinal protozoan parasites, Giardia lamblia and Entameoba histolytica are the most common parasites and are considered to be responsible for acute diarrhea in children [3] [4]. G. lamblia is responsible for about 280 million human cases of diarrhea every year annually [5]. E. histolytica is one of the most important intestinal protozoa in terms of morbidity and mortality, annually infecting about 500 million cases, causing clinical disease of amoebic dysentery and invasive amebiasis in about 50 million and killing about 100,000 individuals [6].
Intestinal worms and soils transmitted helminths reached up to 12% of the total disease burden in children aged 5 - 14 years in low-income countries [7]. Soil-transmitted helminth (STH) infections, caused by A. lumbricoides, T. trichiura and hookworms, are the most predominant and have been recently estimated to affect more than two billion people [8].
The risk factors that maintain the persistence of the prevalence of intestinal parasite infection are poor hygiene conditions, environmental fecal contamination and the lack of sanitary infrastructure, and low access to improved water sources [3] [9].
To reduce morbidity and mortality related to intestinal parasitic infections, several strategies are proposed. WHO recommends integrated approaches 1) preventive chemotherapy (PC), consisting of periodic administration of anthelmintic medicines, 2) improvement of water, sanitation and hygiene (WASH) and 3) behavior change.
In Senegal, intestinal parasitic infection is endemic and children are most affected. Previous studies showed a high prevalence of these diseases [10] [11] [12]. The Ministry of Health has adopted the WHO recommendation which is the implementation of preventive chemotherapy campaigns with Mebendazole or Albendazole [13]. This strategy has significantly reduced the morbidity related to intestinal parasitic infection.
Several years after implementation of mass preventive chemotherapy, an update on the epidemiology of intestinal parasitic infection is important. It was in this context this study was performed with the objective of the prevalence of intestinal parasitic infection in children attending the laboratory of Parasitology-Mycology of Fann Teaching Hospital.
2. Materials and Methods
2.1. Study Design and Population
We carried out a retrospective analysis from January 2016 to December 2020 in the Laboratory of Parasitology-Mycology of Fann University Hospital, which is a public referral hospital, located in the capital city of Dakar. Preschool and school-aged children attending to the laboratory during study period for a parasitological examination of stool samples were included in this study. To be included in the analysis, only children with complete data were considered.
2.2. Data Collection
Sociodemographic, clinical, and biological data from patients were collected using the laboratory records. The following variables were collected: age, sex, year of sample collection, season, clinical indication, parasitological results. Age was defined in 3 categories: less than 5 years, 5 - 10 years, and more than 10 years. The season was defined in both the dry season (October to June) and rainy season (July to September).
2.3. Parasitological Examination
For each child, stool samples were collected using clean wide mouth. After collection, samples were examined macroscopically for color, consistency, presence of blood, mucus, pus, and large worms. Microscopic examination was performed using a proportion of stool samples. Direct examination was processed using light microscopy and the formol-ether concentration technique was used to detect the presence cysts, trophozoite, eggs and larva. The preparation was examined microscopically using the 10× and/or 40 × objectives. The remaining part of stool samples was examined using a modified Zielh Neelsen technique.
2.4. Data Analysis
After data collection, data were entered in Excel software and the analysis was performed using Stata software version MP 16 software. Quantitative variables were described in terms of means, standard deviation. For descriptive data, percentage with confidence interval (CI) was used to assess the prevalence of each outcome. Proportions were compared using chi-square test or the Fisher exact test (univariate analysis). Risk factors were assessed by multivariate survey logistic regression models. Significance level of the different tests was 0.05 two-sided.
2.5. Ethical Considerations
Data are routinely collected from patients who attended to hospital for biomedical testing. Before analysis the data, a permission was requested from the administration of the Hospital. This study was conducted according to the Declaration of Helsinki and existing national legal and regulatory requirements. To respect the confidentiality, an identification code was given to each participant.
3. Results
3.1. Socio-Demographic Characteristics of Preschool and School Aged Children
Au total of 1603 preschool and school-aged children were included in the analysis. Age ranged from 0.5 to 15 years. The mean age of study participant was 6.9 ± 2.4 years. Study population was mainly represented by children age from 5 to 10 years old (78.6%). Children under 5 years old represented 11.2%. Most of study populations are male (54.6%). The sex ratio was 1.2. According to the season, 76.4% of the sample was collected during the dry season against 23.6% during the wet season (Table 1).
3.2. Prevalence of Intestinal Parasitic Infection among Preschool and School-Aged Children
Out of the 1603 children, 429 (26.7%) were found infected with at least one intestinal parasite species. Single infection was noted with a frequency of 83.7% against 16.3% for mixed infections. Protozoa parasites represent 93.9%. Helminth parasites represented 4%. Association between protozoan and helminth was observed in 2.1% (Figure 1).
The most prevalent parasites were Blastocystis sp. (34%), Entamoeba Coli (28%), Giardia intestinalis (9.6%), Endolimax nana (4.9%) and Ascaris lumbricoides (3.5%). Entamoeba histolytica was observed with 1.9%. The other parasites identified were: Pseudolimax butschili (0.5%),Oocyste Isospora belli (0.5%).Trichomonas intestinalis,Chilomastix meslini, Trichuris trichura and Teania were found with 0.2% respectively.
The most common associations were: E Coli + Blastocystis sp. (6.3%), E Coli + E nana (3.3%), G intestinalis + Blastocystis sp. (1.9%), Blastocystis sp + A. lumbricoides (0.5%), G. intestinalis + A. lumbricoides (0.5%). Polyparasitism was noted: A lumbricoides +G intestinalis +Blastocystis sp.,A lumbricoides +E Coli +E Nana,G intestinalis +A lumbricoides +Trichuris trichura,G intestinalis
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Table 1. Socio-demographic characteristics of study participant (N = 1603).
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Figure 1. Prevalence of intestinal parasitic infection (IPI) among study population.
+Blastocystis sp +E Coli andBlastocystis sp + E. coli + E. histolytica. One case of each was noted (Table 2).
Blastocystis sp. was more frequent in children aged over 10 years 24 (15.8%) while E. coli was higher in children aged from 5 to 10 years 146 (11.6%). The frequency of G. intestinalis was more important in children under 5 years 12 (6.7%) than in other age groups. A. lumbricoides was more observed in children aged over 10 years (1.8%) but the difference was not significative between other age groups. Regarding the gender, Blastocystis sp and A. lumbricoides carriage were more important in male subjects. E. coli,G. intestinalis and E. nana were more frequent in female. According to the season, Blastocystis sp. frequency was higher in rainy season (12.9%) than in dry season (11.7%) without any difference
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Table 2. Intestinal parasites species identified among preschool and school-aged children (N = 429).
(p value = 0.5). E. coli and E. Nana were also more observed in rainy season. The frequency of G. intestinalis and A. lumbricoides was more important in dry compared to dry season. When looking the distribution of parasite species according to the presence of symptoms or not, the results of our study showed that Blastocystis sp, E. coli, G. intestinalis, E. nana and A. lumbricoides are more frequent in asymptomatic children (Table 3).
Figure 2 describes the evolution of the prevalence according to the month. Overall, an increase of intestinal parasite prevalence was observed from January to December. Low prevalence rate was noted in January, march and July with 14.9%, 22.7% and 20.6% respectively. High prevalence rate was observed in August (36.9%), October (39.4%) and November (33.3%).
According to the symptomatology 49.2% of study population was symptomatic. Among them, the positivity was 25.1%. The main clinical symptoms were diarrhea, abdominal pain, fever, dyspeptic disorder, and cough. In patients with
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Table 3. Prevalence of different intestinal parasites (Single infection + Mixed infection) according to age groups, gender, season, and symptomatology among preschool and school-aged.
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Figure 2. Monthly evolution prevalence of intestinal parasitic infestations from January 2016 to December 2020.
diarrhea, the prevalence of intestinal parasite was 28.6% (HIV positive with chronic diarrhea), 29% (patients with acute diarrhea, and 16.4% (HIV negative with chronic diarrhea). In patients presenting constipation, fever and dyspeptic disorders, the positivity rate was 33.3%, 32.1% and 32.2% respectively (Table 4).
3.3. Risk Factors Associated with Intestinal Parasitic Infection among Preschool and School-Aged Children
An association between intestinal parasite carriage and age group was noted in this study. Children in age group 5 - 10 years and those aged over 10 years old had high risk of developing intestinal parasite infection with prevalence of 28.1% (aOR = 1.91, 95% CI [1.25 - 2.89] p = 0.002) and 27.4% (aOR = 1.92, 95% CI [1.07 - 3.07] p = 0.002) compared to children under 5 years where the prevalence was 16.7%. According to the year of sample collection, sample collected in 2017, 2019, and 2020 had higher risk for being positive. Prevalence in 2017 was 32.6% (aOR = 1.49, 95% CI [1.11 - 2.01], p = 0.007). In 2019 and 2020, intestinal parasite prevalence was 28.2% (aOR = 1.27, 95% CI [0.88 - 1.84], p = 0.19) and 28.8% (aOR = 1.31, 95% CI [0.83 - 2.08], p = 0.24) respectively.
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Table 4. Prevalence of different intestinal parasites according to clinical symptoms of study participant.
The results from the analysis showed that gender, season and symptom were not correlated with intestinal parasite carriage. Female participants (27.4%) were more affected than male (26.3%) (p = 0.87). Parasite carriage was higher in dry season (26.8%) compared to rainy season (26.5%) without significant difference (p = 0.85). Intestinal parasite prevalence was more important in asymptomatic children (28.3%) (Table 5).
4. Discussion
Intestinal parasitic infections are one of the leading causes of morbidity and mortality in children, especially in those living developing countries. Updating the epidemiology of IPIs is an important epidemiological tool in better guiding existing or new intervention interventions. This study was conducted with the objective of evaluating the prevalence of intestinal parasitic infection in children attending to the laboratory of Parasitology-Mycology of Fann teaching hospital. In this study, the overall prevalence of intestinal parasitic infection was 26.7%% (429/1603). Protozoa were predominant (93.9%) than helminths (4%). Mixed infections represented 2.1%. The most prevalent parasites were Blastocystis sp. (34%), E. coli (28%), G. intestinalis (9.6%), E. nana (4.9%) and A. lumbricoides
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Table 5. Risk factors associated with intestinal parasitic infection among preschool and school-aged children.
(3.5%). E. histolytica was observed with 1.9%. These results confirm the frequency of intestinal parasitic infection in children living in Senegal with a high proportion of protozoa. Since mass preventive campaign with Mebendazole or Albendazole, a significant decrease of helminths wad noted. Similar results were described in Senegal by other authors. Sylla et al. when studying the epidemiological aspects of intestinal parasitic infection in the same hospital between, have found a prevalence of 26.8% with a predominance of protozoa (83%). Parasite species isolated were E. coli (58.9%), E. nana (10%), G. intestinalis (7.1%), A. lumbricoides (9.4%) [11]. Tine et al. in 2013 have reported 26.2% of prevalence for intestinal parasites with a predominance of protozoa in children under five years. Parasites species were represented by G. intestinalis (15.6%), E coli (10.9%), Hymenolepis nana (1.9%), A. lumbricoides (9.4%) and Enterobius vermicularis 0.4% [12]. Sylla et al. during a study evaluating the epidemiological profile of intestinal parasitic infection among children living in a rural community have found 35% prevalence. Protozoa were mainly represented (93.4%) than helminths (2.2%). Association between protozoan and helminth was observed in 4.4%. Parasites observed were G. intestinalis (72.48%), E. coli (13.76%), Blastocystis sp (3.67%) and H. nana (1.83%) [14]. Diouf et al. have demonstrated high prevalence of intestinal parasites (31.3%) with high proportion of protozoa. G. intestinalis (45.3%), E. coli (13.9%) and A. lumbricoides (31.4%) were the most prevalent parasites [15]. Low prevalence (15.8%) was noted by Diongue et al. when assessing the distribution of parasites detected in stool samples in Dakar. Monoparasitism represented 85.7% and mixed infection 14.3%. The most common parasites detected were E. coli (38.9%), E. histolytica/dispar (12.7%), G. intestinalis (8%), and A. lumbricoides (7.3%) [16]. Other studies carried out in the sub-region have shown that intestinal parasitic infections are frequent in the populations. This was demonstrated in Guinea by Beavogui et al. who showed 19.1% prevalence of intestinal parasite children. The main parasites identified were Entamoeba coli (5.4%) and Giardia intestinalis (5.1%) [17]. High prevalence was observed in Burkina Faso with important proportion of intestinal protozoa (84.7%), while helminths represented 10.7%. The predominant species were E. histolytica/E. dispar (66.5%), by Entamoeba coli (37.4%), G. intestinalis (28.1%), and Trichomonas intestinalis (23.4%). The most predominant helminth was H. nana (6.5%) [18]. In Gabon, M’bondoukwé et al. have noted 61.1% prevalence of intestinal parasites including intestinal protozoa (56.7%) and soil-transmitted helminths (22.2%). The most common IPI was Blastocystis. sp (48.6%), A. lumbricoides (13.7%), T. trichura (11.8%), E. histolytica (9.3%), G. intestinalis (4.8%), and Strongyloides strercolaris (3.7%) [19].
Similar result was found in Madagascar with high prevalence (93.6%) of intestinal parasites. The most prevalent parasites were Giardia intestinalis (79.5%), Ascaris lumbricoides (68.3%) and Trichuris tri- chiura (68.0%) [20]. In Ethiopia, Telanesh et al. when assessing the prevalence of intestinal parasitic infection in children under 5 years have noted that 17.4% were infected. Protozoa parasite represent 14.2% (G. intestinalis 8.5%, E. histolytica 5.7%) [21]. Low frequency of helminths parasites was noted (3.2%): tree A. lumbricoides, four T. trichura and one Taenia [22]. The endemicity of intestinal parasitic infection in children was previously described in India where Deka et al. have found 36.6% prevalence. In this study helminths were more common than protozoa [23]. Our study showed that the prevalence of intestinal parasitosis increases significantly with age. In children under 5 years old, the prevalence was 16.7%. This prevalence was higher in children aged 5 to 10 years (28.1%) and those aged over 10 years of age (27.4%). These results are in line with what previously described by Sylla et al. in and Diouf et al. in Kaolack [14] [15]. Regarding the gender, high prevalence IPIs was noted in female subjects (27.4% compared to male subjects (26.3%), but no significant difference. Similar results were noted by Sylla et al. in Senegal (36.8% in female against 33.2% in male) and Telanesh et al. in Ethiopia (23 case in female against 20 in male) [14] [18]. In others studies intestinal parasitic infection prevalence was more important in male than female. This was demonstrated in Burkina Faso and in Kenya [18] [23]. Intestinal parasitic infection was more frequent during the dry season (26.8%) compared to rainy season (26.9%) (p = 0.85). This situation is related to fact that dry season is longer than rainy season. In another study conducted by Sylla et al. in 2013, intestinal parasite prevalence was higher frequency in rainy season (27.27%) than in the dry season 26.5% [11]. The results of our study showed that intestinal parasite prevalence was more frequent in asymptomatic subjects (28.3%) compared to symptomatic ones (25.1%). Most common symptoms in symptomatic children were diarrhea, abdominal pain, fever, dyspeptic disorder, and cough. Similar results were found in Guinea where main symptoms noted in children included abdominal bloating (35%), fever (30.4%), and cough (16.8%), and abdominal pain (4.1%) [17].
Study Limitations
In Senegal, health facilities are not regularly frequented by communities because of financial and geographic accessibility. Laboratory testing of intestinal parasite confirmation are not often prescribed. People are often use systematic deworming instead of going to hospital. In addition, the source of data (laboratory records) and study design (retrospective study in a hospital setting) are some limitations of our study. All these factors probably led to underestimate the prevalence of intestinal parasitic infections.
5. Conclusion
Intestinal parasitic infection is frequent in preschool and school-aged children with a high proportion of protozoa parasites. Low prevalence of helminth parasites could be explained by the effect of mass preventive treatment with Mebendazole or Albendazole. Additional preventive measures such as improved hygiene conditions and health education for the children could reduce transmission and re-infection of children.
Funding
This study was not funded. Funding for data collection was covered by the Laboratory of Parasitology-Mycology, of Fann Teaching Hospital.
Acknowledgements
We would like to acknowledge the entire study participant and the staff of the laboratory of parasitology at Fann Teaching Hospital.
Authors’ Contributions
Khadime Sylla conceived and designed the study. Khadime Sylla supervised the data collection. Khadime Sylla analyzed the data and wrote the first draft of the manuscript. All authors read and approved the final manuscript.
Availability of Data and Material
The data used for this research article are available from the corresponding author upon request.